Effects of early-life cecal microbiota transplantation from divergently selected inbred chicken lines on growth, gut serotonin, and immune parameters in recipient chickens

Authors: FU, YUECHI - Purdue University; HU, JIAYING - Purdue University; ERASMUS, MARISA - Purdue University; JOHNSON, TIMOTHY - Purdue University; Cheng, Heng-Wei

Submitted to: Poultry Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2022
Publication Date: 7/1/2022
Citation: Fu, Y., Hu, J., Erasmus, M.A., Johnson, T.A., Cheng, H. 2022. Effects of early-life cecal microbiota transplantation from divergently selected inbred chicken lines on growth, gut serotonin, and immune parameters in recipient chickens. Poultry Science. https://doi.org/10.1016/j.psj.2022.101925.
DOI: https://doi.org/10.1016/j.psj.2022.101925

Interpretive Summary: Aggressive injury is a critical welfare concern in poultry, leading to feather damage, severe injuries, and even death. Developing a reliable method to control aggression is necessary for improving chicken health and welfare. Fecal microbiota transplantation exerts beneficial effects on modulating health in patients with gastrointestinal dysfunction or with symptoms associated with neurodegenerative and neuropsychiatric disorders. The aim of this study was to examine if cecal microbiota transplantation presents similar efficiency in improving health and welfare status in chickens. To test the hypothesis, the divergently selected inbred chicken lines 63 (gentle birds) and 72 (aggressive birds) were used as donors and a commercial chicken line was used as recipients. The results indicate that early postnatal cecal microbiota transplantation has the potential to reduce aggressive behaviors and improve health in chickens through regulating the gut-immune-brain axis. The findings may provide insights for egg producers and animal scientists to develop novel management strategies for improving poultry health and welfare.

Technical Abstract: Fecal microbiota transplantation exerts beneficial effects on modulating stress-related inflammation and gastrointestinal health and neuropsychiatric disorders in humans. The aim of this study was to examine if cecal microbiota transplantation (CMT) presents similar efficiency in improving health status in chickens. Chickens from the lines 63 and 72 divergently selected for resistance or susceptibility to Marek’s disease were used as CMT donors. Eighty-four d-old male recipient chicks (from a commercial DeKalb XL layer strain) were randomly assigned into 1 of 3 treatments with 7 replicates per treatment and 4 birds per replicate (n=7): CTRL (a saline solution, control), 63-CMT (a cecal solution from line 63), and 72-CMT (a cecal solution from line 72) for a 16-wk trial. Cecal transplant gavage was conducted once daily from day 1 to day 10, then boosted once weekly from week 3 to week 5. The results indicated that 72-CMT recipient birds had the heaviest body weight and the highest ileal villus/crypt ratio among the treatments at week 5 (P = 0.05); and higher heterophil/lymphocyte ratios than that of 63-CMT recipient birds at week 16 (P < 0.05). 72-CMT recipient birds also had higher levels of plasma natural immunoglobulin G and Interleukin (IL)-6 at week 16. In contrast, 63-CMT recipient birds had higher concentrations of ileal mucosal secretory IgA at week 5 and plasma IL-10 at week 16 (P < 0.05), with a tendency for decreased mRNA abundance of IL-6 and Tumor necrosis factor-a in the spleens at week 16 (P = 0.08 and 0.07, respectively). In addition, 72-CMT recipient birds tended to have the lowest serotonin concentrations (P = 0.07) with the highest serotonin turnover in the ileum at week 5 (P < 0.05). There were no treatment effects on the levels of plasma corticosterone and testosterone at week 16 (P > 0.05). In conclusion, early postnatal CMT from different donors leads to different patterns of growth and health status in recipient chickens via the regulation of ileal morphological structures, gut-derived serotonergic activities, peripheral cytokine, and antibody production.